Notes
KURSAR, T. A., H. SWIFT, AND R. S. ALBERTE. 1981.
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and
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L. W. Haas
D. Hayward
Virginia Institute of Marine
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Limnol
Oceanogr.,
28(6). 1983, 1231-1237
Society of Limnology
CC 1983, by the American
and Oceanographb,
1231
Submitted:
Accepted:
27 May 1982
18 April 1983
Inc
The time-course of uptake of inorganic and organic nitrogen
compounds by phytoplankton
from the Eastern
Canadian Arctic: A comparison with
temperate and tropical populations
Abstract-Uptake
of inorganic (NO,-, NH,‘)
and organic (urea) nitrogen compounds by arctic phytoplankton
was linear for at least 30 h
of incubation under natural temperature
and
light conditions. Extrapolation
of linear fits of
the data showed positive ordinal intercepts for
NH,‘, suggesting relatively more rapid uptake
early in the incubation period. Short term uptake experiments confirmed this; rates computed from 20-min incubations were on the average 3-fold higher than 24-h uptake rates. The
transient nature of these enhanced uptake rates
resulted in their contributing
little (~10%) to
the total mass flux observed over 24 h. Comparison of these experiments with similar measurements from temperate and tropical waters
suggests that the often observed nonlinearity
in
nitrogen uptake in the field may be more a
consequence of isotope dilution and recycling
than substrate exhaustion.
Recent research on the relationship between nitrogen uptake and growth in marine algae has suggested that the long es-
1232
Notes
tablished steady state conceptual models
(Dugdale 1967) may no longer be adequate. The mechanisms by which phytoplankton exploit highly variable (in space
and time) nutrient environments are now
considered by many to be ecologically
most relevant (e.g. McCarthy and Goldman 1979). Studies with continuous cultures, for example, have shown that nutrient uptake is substantially elevated and
uncoupled from growth when nitrogendepleted algae are presented with the limiting substrate in discrete pulse additions
(e.g. Conway and Harrison
1977; McCarthy and Goldman 1979; Goldman and
Glibert 1982). These findings imply that
the most important
physiological
time
scales for nitrogen utilization
by N-limited natural phytoplankton
assemblages are
of the order of minutes or less (Goldman
et al. 1981; Goldman and Glibert 1982)
and that conventional experimental methods, usually scaled to hours or longer, may
obscure such short term responses.
Field studies in temperate coastal waters
have shown that phytoplankton
can take
up NH,+ rapidly and that the magnitude
of this enhanced uptake is inversely related to environmental
levels of NH,’ (Glibert and Goldman 1981). These enhanced
uptake rates, however, are apparently
transient phenomena and decrease rapidly with time. This, added to similar
problems of nonlinear
uptake resulting
from substrate depletion during long bottle incubations, has seriously complicated
the interpretation
of conventional
methodology (Goldman et al. 1981).
Near-surface waters in the Eastern Canadian Arctic are typically
low in dissolved inorganic
nitrogen
compounds
during summer when most phytoplankton production occurs (e.g. Harrison et al.
1982) and, despite low seawater temperatures and relatively low incident radiation,
nutrient limitation
has been considered
important
in regulating
phytoplankton
growth in the region (Nemoto and Harrison 1981). In preliminary
studies of nitrogen and phosphorus utilization
(using
conventional methodology, i.e. 24-h incubations) in northern Baffin Bay we found
no evidence of severe nutrient limitation
(Harrison et al. 1982). However, no measurements have been made to date to assess the capacity of these low nutrient
populations for rapid nitrogen uptake nor
to investigate the more general time dependence of uptake during long incubations. I made such time-course measurements of nitrogen uptake during a cruise
to the Canadian Arctic in August 1980 and
compared them with results of similar experiments from temperate and tropical
ocean waters.
Samples were collected from the sea
surface (bucket) or pumped from the
sampling depth (progressive cavity pump:
Herman et al. unpubl.) and immediately
dispensed into transparent glass bottles for
tracer experiments;
samples were not
prescreened for zooplankton. Subsamples
were processed for dissolved nutrients at
sea within an hour of collection and for
particulate
materials later at the laboratory. Nitrogen uptake rates were determined by the ‘“N tracer method of Dugdale and Goering (1967). To 0.5~liter
samples, ‘jKN0, (99 atom%), (‘“NH,),SO,
(99 atom%), or [15N]urea (95 atom%) were
added to bring the final tracer addition to
0.1 pg-atom *liter-l. Samples were collected for analysis after varying periods of
incubation from 20 min to 30 h. After incubation,
the 15N-enriched
particulate
matter was harvested on precombusted
Whatman GF/F glass filters and rinsed
with filtered seawater. 15N:13N ratios were
determined
by emission spectrometry
(Fiedler and Proksch 1975). Carbon and
phosphorus uptake rates were determined
after adding -“5 &i HlCO,or carrierfree [33P]phosphoric acid to 25O-ml samples. Particles in these experiments were
also collected on glass-fiber filters after incubation and assayed for radioactivity
by
scintillation
spectrometry.
All tracer experiments were done in clear acrylic deck
boxes, exposed to natural sunlight and
cooled with near-surface flowing seawater. Additional
particulate
samples were
analyzed for Chl a (Holm-Hansen
et al.
1965) and particulate
organic nitrogen
(Sharp 1974). Filtrates were used for analysis of dissolved nutrients: NO,?-, NH,+,
and PO,“- (Strickland and Parsons 1972)
Initial
3
4
5
Sep 80
36”58’N, 75=‘53’W
40”38’N, 7 1”03’W
Mar 80
9”24’N, 89”36’W
Jul
Jul
Jul
Aug
Aug
Aug
Aug
Aug
Aug
Aug
environmental
56”26’W
64”32’W
69”09’W
69”04’W
69’5O’W
81”48’W
86’=03’W
86”lO’W
8 l”35’W
81”06’W
Location
67”22’N,
74”55’N,
75”46’N,
75”54’N,
75”22’N,
73”53’N,
74”26’N,
74”21’N,
73”59’N,
73”48’N,
Initial
1
4
1
1
1
1
1
1
1
1
8.0
2.2
2.5
2.5
4.0
4.8
4.5
5.0
5.2
5.0
conditions
1
1
1
25
25
conditions
~2.7
~2.3
~2.3
1.7
2.0
experiments.
1.00
3.36
0.27
0.90
2.06
Chl
33.3
18.1
10.8
11.3
24.4
PON?
Biomass (mg.mm3)
time-course
0.84
0.10
0.11
0.20
0.21
NH,+
1.21
0.21
0.24
0.06
1.76
NO,-
Nutrients
41
62
10
52
38
74
32
48
38
19
0.24
0.17
0.27
0.03
0.14
0.03
0.03
0.03
0.37
0.17
smce nonbiologrcal
1.52
0.40
0.58
0.35
0.21
0.23
2.96
0.15
0.18
0.69
uptake
of “NH,
1030
1530
0950
1040
1130
1350
1240
1000
0930
1200
* is generally
0.303
0.285
0.051
0.066
0.050
0.108
0.295
0.096
0.105
0.089
1,1+
negligible
0.418
0.311
0.058
0.076
0.067
0.333
0.318
0.120
0.161
0.117
2.25
0.69
1.33
1.17
1.91
2.15
2.59
1.33
2.89
1.35
(b) 24 h
excess)
(e.g Clibert
(atom%
(a) 20 min
15N enrichment
0.72
0.18
0.26
0.92
1.13
PO,?-
and Goldman
0.0246
0.0103
0.0028
0.0013
0.0027
0.0121
0.0049
0.0024
0.0145
0.0042
1981)
(c) 20 min*
15N uptake
0.0032
0.0008
0.0020
0.0006
0.0019
0.0012
0.0014
0.0007
0.0057
0.0015
(d) 24 h
rate (h-l)
Eastern Canadian
-
-
0.21
0.45
Urea
(mg-atoms.mm3)
and NH,+ uptake rates for short term (20 min) 15N experiments,
28
26
23
4
5
(ac,
for extended
* Incident solar radiation
(PAR) d urine, short term experiments
t Nominal
filtering
times for t,, (time-zero)
samples were ca 5 min
$ Time-zero
enrrchments
were not subtracted
for these computations
27
29
31
1
3
5
6
7
9
12
Date
(1980)
Table 2.
* Daily incident radiation
(PAR)
t Particulate
organic nitrogen.
1
2
EXP
No.
environmental
Aug 80
74”57’N, 78”08’W
74”39’N, 88”48’W
Location
Table 1.
7.7
12.9
1.4
2.2
1.4
10.1
3.5
3.4
2.5
2.8
c/d
Arctic.
18.6
45.1
4.4
6.5
3.5
15.5
12.3
9.0
5.6
8.7
a/b
(%)
0900
1300
0900
1200
1400
Timezero
(local)
1234
Notes
4AUG60
LOCAL
TIME
5AUG80
16AUG80
LOCAL
TIME
Ii’AUG 60
Fig. 1. Time-course measurements of nutrient uptake in the Eastern Canadian Arctic. A. 4 August 1980.
B. 16 August 1980. Environmental
conditions at time-zero given in Table 1. I, = daily incident radiation,
PAR. (A is redrawn from Li and Harrison 1982.)
and urea (McCarthy
1970). Solar radiation was recorded hourly with a LiCor LI192s quantum sensor (PAR) coupled to an
integrator (LiCor LI 550).
CO=--<--
INCUBATION
TIME
( h )
Fig. 2. Short term uptake of NH,’ and POb3- in
the Eastern Canadian Arctic, 13 August 1980. Sample from 5-m depth, time-zero = 1445 hours, amwere 0.28 and
bient NH,’ and POd3- concentrations
0.80 mg-atoms.m- 3. 15NH,+ added at two concentration levels, 0.1 (dashed line) and 10 kg-atoms.liter-’
(solid lines).
Two extended time-course experiments
in northern Baffin Bay (Table 1) showed
that all forms of nitrogen (NO,-, NH3+,
urea) seemed to be taken up at a constant
rate for at least 30 h (Fig. 1). Patterns for
PO,?- and HCO,- uptake were similar despite marked diel variation in solar radiation. Li and Harrison (1982) have attributed the relative light independence
of
HCO,- uptake to the low irradiance levels
required to saturate photosynthesis in these
high latitude populations. I found the same
pattern in experiments on N uptake vs.
light (unpubl. data). Linear regressions of
nitrogen uptake vs. time were highly significant
(P < 0.001) but did not pass
through the origin; positive ordinal intercepts were apparent in most cases and
were statistically significant (P < 0.10) for
NH,‘. Higher resolution sampling confirmed this (Fig. 2) and suggested that
rates of 13NH1+ uptake were highest for
short incubations. A comparison of uptake
rates computed from 20-min and 24-h incubations from several locations in the
Eastern Arctic showed that short term uptake rates were substantially greater than
long term estimates; uptake ratios ranged
from I.4 to 12.9 with a median value of
3.1 (Table 2). However, these enhanced
rates were not sustained; ‘“N accumulation by the particulate matter during the
Notes
6
24
INC”E&ION
TlME’*t
30
h)
1235
6
24
INC”Bh:ION
TlME’“(
30
h)
Fig. 3. Relationship between incubation time and
15N enrichment
of the particulate
matter. Symbols
correspond to experiments listed in Table 1: O-No.
1; A-No.
2; O-No.
3; A-No.
4; X-No.
5.
Fig. 4. Relationship between NH,+ uptake rate
(as fraction of l-h rate) and incubation time; arctic
experiments (No. 1, 2) and temperate experiments
(No. 3, 4) of Table 1.
first 20 min of incubation generally represented ~10% of the 24-h accumulation.
Others have documented transient, elevated NH,’ uptake rates in phytoplankton populations
from temperate waters
(Goldman et al. 1981; Glibert and Goldman 1981; Wheeler et al. 1982). In contrast to my findings for the arctic, however, these other data showed that a
substantial portion (often >50%) of the 15N
accumulation
occurred in the first lo-20
min of incubation.
Time-course
experiments
comparable
to those in the arctic made in temperate
and tropical
ocean waters (Table 1)
showed highly nonlinear
NH,’
uptake
(Fig. 3). Uptake rates computed
from
24-h incubations represented only about
5% of the I-h values for the temperate
data in the extreme case; 24-h rates were
~80% of the l-h rates for the arctic data
(Fig. 4).
I did a statistical (correlation)
analysis
of environmental
conditions
associated
with each time-course experiment (Tables
1 and 2) in an effort to explain the interand intraregional
differences in the time
dependence of NH,+ uptake. Variation in
no single environmental
parameter was
entirely consistent with the observed patterns in NH,+ uptake within regions, although temperature clearly differentiated
results among regions. NH,+ uptake patterns, for example, were markedly different for arctic and temperate experiments
despite comparable
levels of substrate
(NH,‘)
and particulate
biomass (Chl,
PON).
The possibility that greater light dependence of NH,’ uptake contributed
to the
observed nonlinear pattern in the lower
latitude experiments was considered, since
all studies were done under natural lightdark cycles. However, the facts that independently measured “dark bottle” NH,+
uptake was generally ~75% of the “light
bottle” NH,+ uptake rates, ‘jN uptake rates
in the time-course studies did not increase
on exposure to light following
the dark
period, and nonlinearity
of uptake was
apparent well before the onset of darkness
suggested that light dependence had little
effect on the observed nonlinear uptake
patterns. Nonphotosynthetic
microorganisms (i.e. bacteria) can be important in inorganic-N utilization
(Cuhel et al. 1983);
however, their relative importance in the
present study was not assessed.
Substrate exhaustion during prolonged
incubation
has been considered a major
cause of nonlinear uptake rates in field
measurements
(Goldman
et al. 1981).
However, this does not seem to be an adequate explanation
for my results. According to computations
using measured
concentrations and 13N enrichment levels
of the substrate and particulate nitrogen,
only about 30-40% of the lsNH,+ available
was taken up during any of the timecourse experiments.
Nor is this expla-
1236
Notes
Fig. 5. Relationship between nonlinearity of NH,+
uptake (T,,-time
required to reach 50% maximum
attained 15N enrichment) and substrate (NH.,+) turnover time. Turnover
times computed with uptake
rates determined from linear portion of time-course
experiments. Symbols as in Fig. 3.
nation satisfactory
when one considers
recent evidence of substantial NH,’ production within
incubation
bottles (e.g.
Harrison 1978; Glibert 1982).
Alternatively,
the observed nonlinear
uptake patterns could be explained by isotopic exchange, isotope dilution,
or biologically
mediated
recycling
(e.g. via
grazing). Isotopic exchange between external and intracellular
nutrient pools can
account for the apparent rapid uptake of
some inorganic nutrients by phytoplankton (e.g. PO:-: Nalewajko and Lean 1980).
This, however, has not been a satisfactory
explanation for short term enhanced uptake of NH,+ observed in the field and in
cultures; intracellular
NH,+ pools are generally too small in marine phytoplankton
to accommodate the large isotope fluxes
measured (Wheeler et al. 1982; Goldman
and Glibert 1982).
Glibert et al. (1982b) have shown that
isotope dilution, resulting primarily
from
microplankton
excretion
of unlabeled
NHJ+, may contribute substantially to the
nonlinear NH,’ uptake pattern observed
over longer incubations. More recent studies in our laboratory confirm this but also
suggest that recycling of previously assimilated ljNH,+ may be important when uptake and regeneration fluxes are high, i.e.
when substrate turnover times are short
(see also Harrison 1983). A strong correlation between substrate turnover time and
the degree of nonlinearity
in NH,+ uptake
observed in the experiments
described
here (Fig. 5) lend indirect support to the
importance of isotope dilution and recycling in explaining the NH,+ uptake patterns. In a more general context, these results suggest that ambient
substrate
concentration
is a necessary (Glibert and
Goldman 1981) but often not sufficient
condition for determining
the time dependence (linearity) of nutrient uptake.
Other more indirect detrimental
bottle
effects (e.g. mortality)
of long confinement of plankton populations have also
been suggested as an important cause of
nonlinear nutrient uptake. Glibert et al.
(1982u), for example, found a time-dependent decrease in nitrogen uptake in
antarctic waters where nutrient levels are
exceedingly high and problems of depletion would be very unlikely. If bottle confinement were a serious problem in the
experiments presented here, then its effects were much more apparent in the
lower latitudes.
In my arctic data, nutrient uptake rates
were linear for at least 30 h despite low
initial substrate concentrations
and relatively high particulate biomass. In this environment,
low temperatures apparently
keep phytoplankton
growth (and thus nutrient demand) at low levels (Harrison et
al. 1982), which tends to lengthen substrate turnover times and significantly
decreases the probability of nutrient exhaustion or isotopic recycling
during long
incubations.
The elevated NH,+ uptake
rates observed in short term experiments,
in contrast to published results from temperate waters, generally represented only
a small fraction of the total mass flux measured over long term incubations. Taken
together, these results support earlier conclusions that phytoplankton in these waters
were not severely nutrient stressed.
W. G. Harrison
Marine Ecology Laboratory
Bedford Institute of Oceanography
Dartmouth, Nova Scotia B2Y 4A2
Notes
References
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4. Transient response of
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limiting nutrient. Mar. Biol. 43: 33-43.
CUHEL, R. L., H. W. JANNASCH, C. D. TAYLOR, AND
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DUGDALE, R. C. 1967. Nutrient limitation
in the
and significance.
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and regenerated forms of nitrogen in primary
productivity.
Limnol. Oceanogr. 12: 196-206.
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spectrometry in biochemical analysis: A review.
Anal. Chim. Acta 78: l-62.
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seasonal and size-fraction
variability
in ammonium remineralization.
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D. C. BIGGS, AND J. J. MCCARTHY. 1982a.
Utilization
of ammonium
and nitrate during
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-,
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1237
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Submitted: 30 November 1982
Accepted: 9 May 1983
Inc
silicon
Abstract-Cosmogenic
32Si has been used as
a tracer to study the behavior of stable silicon
in the Gironde estuary, southwest France, partitularly
to identify the source of excess stable
silicon observed in low salinity areas.
The results indicate that the dissolved 32Sibehaves conservatively
in mixing in the estuary
and that the excess stable silicon found in the
low salinity zone is likely to be anthropogenic.
Knowledge of the flux of dissolved components through rivers to the ocean is important to an understanding of the marine
geochemical balance and to postulating a
steady state model for the ocean (Mackenzie and Garrels 1966u,b). Only a rough
estimate of the riverine flux of dissolved